Age-dependent female responses to a male ejaculate signal alter demographic opportunities for selection

A central tenet of evolutionary explanations for ageing is that the strength of selection wanes with age. However, data on age-specific expression and benefits of sexually selected traits are lacking—particularly for traits subject to sexual conflict. We addressed this by using as a model the responses of Drosophila melanogaster females of different ages to receipt of sex peptide (SP), a seminal fluid protein transferred with sperm during mating. SP can mediate sexual conflict, benefitting males while causing fitness costs in females. Virgin and mated females of all ages showed significantly reduced receptivity in response to SP. However, only young virgin females also showed increased egg laying; hence, there was a narrow demographic window of maximal responses to SP. Males gained significant ‘per mating’ fitness benefits only when mating with young females. The pattern completely reversed in matings with older females, where SP transfer was costly. The overall benefits of SP transfer (hence opportunity for selection) therefore reversed with female age. The data reveal a new example of demographic variation in the strength of selection, with convergence and conflicts of interest between males and ageing females occurring over different facets of responses to a sexually antagonistic trait.

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The genomic footprint of sexual conflict

Nature Ecology & Evolution ◽

10.1038/s41559-019-1041-9 ◽

2019 ◽

Vol 3 (12) ◽

pp. 1725-1730 ◽

Cited By ~ 7

Author(s):

Ahmed Sayadi ◽

Alvaro Martinez Barrio ◽

Elina Immonen ◽

Jacques Dainat ◽

David Berger ◽

...

Keyword(s):

Life History ◽

Sexual Conflict ◽

Callosobruchus Maculatus ◽

Seminal Fluid ◽

Balancing Selection ◽

Molecular Genetic ◽

Purifying Selection ◽

Phenotypic Selection ◽

Genomic Signatures ◽

Seminal Fluid Protein

AbstractGenes with sex-biased expression show a number of unique properties and this has been seen as evidence for conflicting selection pressures in males and females, forming a genetic ‘tug-of-war’ between the sexes. However, we lack studies of taxa where an understanding of conflicting phenotypic selection in the sexes has been linked with studies of genomic signatures of sexual conflict. Here, we provide such a link. We used an insect where sexual conflict is unusually well understood, the seed beetle Callosobruchus maculatus, to test for molecular genetic signals of sexual conflict across genes with varying degrees of sex-bias in expression. We sequenced, assembled and annotated its genome and performed population resequencing of three divergent populations. Sex-biased genes showed increased levels of genetic diversity and bore a remarkably clear footprint of relaxed purifying selection. Yet, segregating genetic variation was also affected by balancing selection in weakly female-biased genes, while male-biased genes showed signs of overall purifying selection. Female-biased genes contributed disproportionally to shared polymorphism across populations, while male-biased genes, male seminal fluid protein genes and sex-linked genes did not. Genes showing genomic signatures consistent with sexual conflict generally matched life-history phenotypes known to experience sexually antagonistic selection in this species. Our results highlight metabolic and reproductive processes, confirming the key role of general life-history traits in sexual conflict.

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Reduced egg laying caused by a male accessory gland product opens the possibility for sexual conflict in a simultaneous hermaphrodite

Animal Biology ◽

10.1163/157075509x12499949744306 ◽

2009 ◽

Vol 59 (4) ◽

pp. 435-448 ◽

Cited By ~ 18

Author(s):

Joris Koene ◽

Jeroen Hoffer ◽

Annelies Brouwer

Keyword(s):

Sexual Conflict ◽

Lymnaea Stagnalis ◽

Seminal Fluid ◽

Accessory Gland ◽

Egg Laying ◽

Simultaneous Hermaphrodite ◽

Internal Fertilization ◽

Sperm Donors ◽

Underlying Mechanisms ◽

Simultaneous Hermaphrodites

AbstractPromiscuity, sperm storage and internal fertilization enhance sperm competition, which leads to sexual conflict whenever an advantageous trait for sperm donors is harmful to recipients. In separate-sex species, such conflicts can severely impact the evolution of reproductive characteristics, physiology and behaviours. For simultaneous hermaphrodites, the generality of this impact remains unclear and underlying mechanisms remain largely unexplored. In the hermaphrodite Lymnaea stagnalis several previous studies showed that investment in eggs differs depending on semen receipt, but these were inconsistent about the direction of change. We investigated whether the change in egg laying is caused by a seminal fluid component. By intravaginally injecting animals, we here reveal that a component of the seminal fluid inhibits egg laying, thus providing the first direct evidence for involvement of such components in competition for fertilization in hermaphrodites. We discuss the broad implications that this finding has on a number of previous studies performed in the same species.

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A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating.

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.92.22.10114 ◽

1995 ◽

Vol 92 (22) ◽

pp. 10114-10118 ◽

Cited By ~ 214

Author(s):

L. A. Herndon ◽

M. F. Wolfner

Keyword(s):

Seminal Fluid ◽

Egg Laying ◽

Seminal Fluid Protein

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Mated Drosophila melanogaster Females Require a Seminal Fluid Protein, Acp36DE, to Store Sperm Efficiently

Genetics ◽

10.1093/genetics/153.2.845 ◽

1999 ◽

Vol 153 (2) ◽

pp. 845-857 ◽

Cited By ~ 1

Author(s):

Deborah M Neubaum ◽

Mariana F Wolfner

Keyword(s):

Drosophila Melanogaster ◽

Seminal Fluid ◽

Sperm Storage ◽

Egg Laying ◽

Limited Area ◽

Seminal Fluid Proteins ◽

Barrier Formation ◽

Storage Organs ◽

Initial Storage ◽

Seminal Fluid Protein

Abstract Mated females of many animal species store sperm. Sperm storage profoundly influences the number, timing, and paternity of the female’s progeny. To investigate mechanisms for sperm storage in Drosophila melanogaster, we generated and analyzed mutations in Acp36DE. Acp36DE is a male seminal fluid protein whose localization in mated females suggested a role in sperm storage. We report that male-derived Acp36DE is essential for efficient sperm storage by females. Acp36DE1 (null) mutant males produced and transferred normal amounts of sperm and seminal fluid proteins. However, mates of Acp36DE1 males stored only 15% as many sperm and produced 10% as many adult progeny as control-mated females. Moreover, without Acp36DE, mated females failed to maintain an elevated egg-laying rate and decreased receptivity, behaviors whose persistence (but not initiation) normally depends on the presence of stored sperm. Previous studies suggested that a barrier in the oviduct confines sperm and Acp36DE to a limited area near the storage organs. We show that Acp36DE is not required for barrier formation, but both Acp36DE and the barrier are required for maximal sperm storage. Acp36DE associates tightly with sperm. Our results indicate that Acp36DE is essential for the initial storage of sperm, and that it may also influence the arrangement and retention of stored sperm.

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Fluctuating selection strength and intense male competition underlie variation and exaggeration of a water strider’s male weapon

10.1101/430314 ◽

2018 ◽

Author(s):

William Toubiana ◽

Abderrahman Khila

Keyword(s):

Mating Behavior ◽

Phenotypic Variation ◽

Male Competition ◽

Egg Laying ◽

Leg Length ◽

Fluctuating Selection ◽

Sexually Selected Traits ◽

Selected Traits ◽

Gravid Females ◽

The Impact

AbstractSexually selected traits can reach high degrees of expression and variation under directional selection. A growing number of studies suggest that such selection can vary in space, time and form within and between populations. However, the impact of these fluctuations on sexual trait expression is poorly understood. The water striderMicrovelia longipesdisplays a striking case of exaggeration and phenotypic variation where males display extreme differences in the size of their rear legs. To study the origin and maintenance of this exaggerated trait, we conducted comparative behavioral and morphometric experiments in a sample ofMicroveliaspecies. We uncovered differences both in the mating behavior and the degree of sexual dimorphism across these species. Interestingly,M. longipesevolved a specific mating behavior where males compete for egg-laying sites, consisting of small floating objects, to intercept and copulate with gravid females. Field observations revealed rapid fluctuation inM. longipeshabitat stability and the abundance of egg-laying sites. Through male-male competition assays, we demonstrated that male rear legs are used as weapons to dominate egg-laying sites and that intense competition is associated with the evolution of rear leg length exaggeration. Paternity tests using genetic markers demonstrated that small males could only fertilize about 5% of the eggs when egg-laying sites are limiting, whereas this proportion increased to about 20% when egg-laying sites become abundant. Furthermore, diet manipulation and artificial selection experiments also showed that the exaggerated leg length inM. longipesmales is influenced by both genetic and nutritional factors. Collectively, our results highlight how fluctuation in the strength of directional sexual selection, through changes in the intensity of male competition, can drive the exaggeration and phenotypic variation in this weapon trait.

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Sexual selection affects the evolution of physiological and life history traits

10.1101/2021.03.23.436586 ◽

2021 ◽

Author(s):

Martin David Garlovsky ◽

Luke Holman ◽

Andrew L Brooks ◽

Rhonda R Snook

Keyword(s):

Sexual Selection ◽

Life History ◽

Sexual Conflict ◽

Life History Traits ◽

Experimental Manipulation ◽

Endurance Capacity ◽

Development Activity ◽

Sexually Selected Traits ◽

Trade Offs ◽

Selected Traits

Sexual selection and sexual conflict are expected to affect all aspects of the phenotype, not only traits that are directly involved in reproduction. Here, we show coordinated evolution of multiple physiological and life history traits in response to long-term experimental manipulation of the mating system in populations of Drosophila pseudoobscura. Development time was extended under polyandry relative to monogamy in both sexes, potentially due to higher investment in traits linked to sexual selection and sexual conflict. Individuals (especially males) evolving under polyandry had higher metabolic rates and locomotor activity than those evolving under monogamy. Polyandry individuals also invested more in metabolites associated with increased endurance capacity and efficient energy metabolism and regulation, namely lipid and glycogen. Finally, polyandry males were less desiccation- and starvation-resistant than monogamy males, suggesting trade-offs between resistance and sexually selected traits. Our results provide experimental evidence that mating systems can impose selection that influences the evolution of non-sexual phenotypes such as development, activity, metabolism, and nutrient homeostasis.

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Sperm Storage Costs Determine Survival and Immunocompetence in Newly Mated Queens of the Leaf-Cutting Ant Atta colombica

Frontiers in Ecology and Evolution ◽

10.3389/fevo.2021.759183 ◽

2022 ◽

Vol 9 ◽

Author(s):

Barbara Baer-Imhoof ◽

Susanne P. A. den Boer ◽

Jacobus J. Boomsma ◽

Boris Baer

Keyword(s):

Serine Proteases ◽

Seminal Fluid ◽

Life Time ◽

Probability Of Survival ◽

Sexually Selected Traits ◽

Mating Costs ◽

Single Mating ◽

Leaf Cutting ◽

Selected Traits ◽

Atta Colombica

In the leaf-cutting ant Atta colombica, queens receive ejaculates from multiple males during one single mating event early in their lives. A queen’s fertility and fitness therefore depend on maximizing the number of sperm cells she can store and maintain inside her spermatheca. Previous studies implied significant physiological mating costs, either originating from energetic investments maximizing sperm survival, or from resolving sexual conflicts to terminate male-driven incapacitation of rival sperm via serine proteases found in seminal fluid. Here we conducted an artificial insemination experiment, which allowed us to distinguish between the effects of sperm and seminal fluid within the queen’s sexual tract on her survival and immunocompetence. We found significantly higher mortality in queens that we had inseminated with sperm, independently of whether seminal fluid was present or not. Additionally, after receiving sperm, heavier queens had a higher probability of survival compared to lightweight queens, and immunocompetence decreased disproportionally for queens that had lost weight during the experiment. These findings indicate that queens pay significant physiological costs for maintaining and storing sperm shortly after mating. On the other hand, the presence of seminal fluid within the queens’ sexual tract neither affected their survival nor their immunocompetence. This suggests that the energetic costs that queens incur shortly after mating are primarily due to investments in sperm maintenance and not costs of terminating conflicts between competing ejaculates. This outcome is consistent with the idea that sexually selected traits in social insects with permanent castes can evolve only when they do not affect survival or life-time fitness of queens in any significant way.

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